Targeting microRNAs as a Therapeutic Strategy to Reduce Oxidative Stress in Diabetes
<p>Graphical representation of oxidative stress mechanisms in β cells. The generation of Reactive Oxygen Species (ROS) could be caused by several conditions including hyperglycaemia, hyperlipidaemia, hypoxia, and Endoplasmic Reticulum (ER) stress (due to inflammation). Increased glucose concentration in β cells stimulates a rapid and proportional rise of glycolytic flux followed by a robust stimulation in the production of reducing equivalents, due to the channeling of glucose carbon into the Tricarboxylic Acid Cycle (TCA) cycle, which can lead to an enhancement of ROS production. However, further increases in intracellular Ca<sup>2+</sup> can stimulate mitochondrial generation of ROS while Ca<sup>2+</sup> via Protein Kinase C (PKC) activation, may enhance Nicotinamide Adenine Dinucleotide Phosphate (NADPH) oxidase-dependent generation of ROS and, thus, induce oxidative stress and/or apoptosis. The mechanism by which Free Fatty Acids (FFAs) promotes ROS generation in mitochondria could be explained by the activation of NADPH oxidase and another mechanism which contributes to lipid-induced oxidative stress in β cells is the modulation of respiratory chain. β cells are also prone to the stress caused by low oxygen levels which leads to ROS production and other signs of oxidative stress. Hypoxia or low oxygen tension can lead to increased ROS generation, mostly through the involvement of complexes I and III of the mitochondrial electron transport chain. In the ER, ROS are generated as a product of protein folding events; therefore, the increased accumulation of dysregulated formation or breakage of disulfide bonds result in an excessive amount of ROS which causes oxidative stress. In addition, the presence of Superoxide Dismutase (SOD), causes the abnormal accumulation of H<sub>2</sub>O<sub>2</sub> and other ROS (green box inset) which may damage the cells at multiple levels.</p> "> Figure 2
<p>3D structure and details of chemical composition of inorganic and organic Nanoparticles (NPs) conjugated to aptamers/nucleic acids. (<b>a</b>) Cerium oxide NP 3D structure is due to the aggregation of several cerium oxide molecules. (<b>b</b>) Gold NPs are modified with Cysteamine (Cys); this modification on gold NP is mainly used to stabilize its binding to the target drug. (<b>c</b>) The hollow 3D structure of a mesoporous silica NP is represented as well; briefly, this structure is composed by a combination of micelles complexed with a silica precursor (SiOH) on the surface of the NP (magnified in the red box). (<b>d</b>) 3D structure of a liposome NP and detailed chemical structure of a single phospholipid composing the membrane of liposome (green box). (<b>e</b>) Chitosan-composed NP is displayed, alongside with the chemical structure of a positively charged chitosan macromolecule on the NH<sub>3</sub> group (green circle). (<b>f</b>) Branched chemical structure and 3D composition of a Polyamidoamine (PAMAM) dendrimer is shown; in the orange box, the typical chemical structure of a PAMAM dendrimer branch is represented.</p> ">
Abstract
:1. Introduction
2. Oxidative Stress in Diabetes
- (i)
- Increased glucose flux and other sugars through the polyol pathway.
- (ii)
- Increased intracellular formation of Advanced Glycation End-products (AGEs).
- (iii)
- Increased expression of receptors for AGEs and its activating ligands.
- (iv)
- Activation of Protein Kinase C (PKC) isoforms and downstream pathways.
- (v)
- Over-activity of the hexosamine pathway [15].
3. miRNAs as Regulators of Oxidative Stress in Diabetes
3.1. miRNAs, β Cell Function and Oxidative Stress
3.2. miRNAs, Oxidative Stress and Diabetic Complications
4. MiRNAs as Therapeutic Targets: Strategies and Perspectives
4.1. miRNA Mimicking or Inhibition
4.2. Delivery Systems for miRNA-Based Drugs
4.2.1. Inorganic Nanoparticles
4.2.2. Organic Nanoparticles (NPs)
4.2.3. Aptamers
4.3. Clinical Advancements of miRNA-Based Drugs
5. Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Zheng, Y.; Ley, S.H.; Hu, F.B. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat. Rev. Endocrinol. 2018, 14, 88–98. [Google Scholar] [CrossRef] [PubMed]
- Lotfy, M.; Adeghate, J.; Kalasz, H.; Singh, J.; Adeghate, E. Chronic complications of diabetes mellitus: A mini review. Curr. Diabetes Rev. 2017, 13, 3–10. [Google Scholar] [CrossRef] [PubMed]
- Winter, J.; Jung, S.; Keller, S.; Gregory, R.I.; Diederichs, S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Biol. 2009, 11, 228–234. [Google Scholar] [CrossRef] [PubMed]
- Nigi, L.; Grieco, G.E.; Ventriglia, G.; Brusco, N.; Mancarella, F.; Formichi, C.; Dotta, F.; Sebastiani, G. Micrornas as regulators of insulin signaling: Research updates and potential therapeutic perspectives in type 2 diabetes. Int. J. Mol. Sci. 2018, 19, 3705. [Google Scholar] [CrossRef] [Green Version]
- Sebastiani, G.; Po, A.; Miele, E.; Ventriglia, G.; Ceccarelli, E.; Bugliani, M.; Marselli, L.; Marchetti, P.; Gulino, A.; Ferretti, E.; et al. MicroRNA-124a is hyperexpressed in type 2 diabetic human pancreatic islets and negatively regulates insulin secretion. Acta Diabetol. 2015, 52, 523–530. [Google Scholar] [CrossRef]
- Sebastiani, G.; Valentini, M.; Grieco, G.E.; Ventriglia, G.; Nigi, L.; Mancarella, F.; Pellegrini, S.; Martino, G.; Sordi, V.; Piemonti, L.; et al. MicroRNA expression profiles of human iPSCs differentiation into insulin-producing cells. Acta Diabetol. 2017, 54, 265–281. [Google Scholar] [CrossRef]
- Sebastiani, G.; Grieco, G.E.; Brusco, N.; Ventriglia, G.; Formichi, C.; Marselli, L.; Marchetti, P.; Dotta, F. MicroRNA Expression Analysis of In Vitro Dedifferentiated Human Pancreatic Islet Cells Reveals the Activation of the Pluripotency-Related MicroRNA Cluster miR-302s. Int. J. Mol. Sci. 2018, 19, 1170. [Google Scholar] [CrossRef] [Green Version]
- Kato, M.; Castro, N.E.; Natarajan, R. MicroRNAs: Potential mediators and biomarkers of diabetic complications. Free Radic. Biol. Med. 2013, 64, 85–94. [Google Scholar] [CrossRef] [Green Version]
- SaeediBorujeni, M.J.; Esfandiary, E.; Baradaran, A.; Valiani, A.; Ghanadian, M.; Codoñer-Franch, P.; Basirat, R.; Alonso-Iglesias, E.; Mirzaei, H.; Yazdani, A. Molecular aspects of pancreatic β-cell dysfunction: Oxidative stress, microRNA, and long noncoding RNA. J. Cell Physiol. 2019, 234, 8411–8425. [Google Scholar] [CrossRef]
- Evans, J.L.; Goldfine, I.D.; Maddux, B.A.; Grodsky, G.M. Oxidative stress and stress-activated signaling pathways: A unifying hypothesis of type 2 diabetes. Endocr. Rev. 2002, 23, 599–622. [Google Scholar] [CrossRef] [Green Version]
- Brownlee, M. The pathobiology of diabetic complications: A unifying mechanism. Diabetes 2005, 54, 1615–1625. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Greenman, I.C.; Gomez, E.; Moore, C.E.J.; Herbert, T.P. Distinct glucose-dependent stress responses revealed by translational profiling in pancreatic beta-cells. J. Endocrinol. 2007, 192, 179–187. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kahn, S.E. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 2003, 46, 3–19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kajimoto, Y.; Kaneto, H. Role of oxidative stress in pancreatic beta-cell dysfunction. Ann. N. Y. Acad. Sci. 2004, 1011, 168–176. [Google Scholar] [CrossRef]
- Giacco, F.; Brownlee, M. Oxidative stress and diabetic complications. Circ. Res. 2010, 107, 1058–1070. [Google Scholar] [CrossRef] [Green Version]
- Newsholme, P.; Haber, E.P.; Hirabara, S.M.; Rebelato, E.L.O.; Procopio, J.; Morgan, D.; Oliveira-Emilio, H.C.; Carpinelli, A.R.; Curi, R. Diabetes associated cell stress and dysfunction: Role of mitochondrial and non-mitochondrial ROS production and activity. J. Physiol. 2007, 583, 9–24. [Google Scholar] [CrossRef]
- Wang, J.; Wang, H. Oxidative stress in pancreatic beta cell regeneration. Oxid. Med. Cell. Longev. 2017, 2017, 1930261. [Google Scholar] [CrossRef] [Green Version]
- Kaneto, H.; Xu, G.; Song, K.H.; Suzuma, K.; Bonner-Weir, S.; Sharma, A.; Weir, G.C. Activation of the hexosamine pathway leads to deterioration of pancreatic beta-cell function through the induction of oxidative stress. J. Biol. Chem. 2001, 276, 31099–31104. [Google Scholar] [CrossRef] [Green Version]
- Sharma, R.B.; Alonso, L.C. Lipotoxicity in the pancreatic beta cell: Not just survival and function, but proliferation as well? Curr. Diabetes Rep. 2014, 14, 492. [Google Scholar] [CrossRef] [Green Version]
- Morgan, D.; Oliveira-Emilio, H.R.; Keane, D.; Hirata, A.E.; Santos da Rocha, M.; Bordin, S.; Curi, R.; Newsholme, P.; Carpinelli, A.R. Glucose, palmitate and pro-inflammatory cytokines modulate production and activity of a phagocyte-like NADPH oxidase in rat pancreatic islets and a clonal beta cell line. Diabetologia 2007, 50, 359–369. [Google Scholar] [CrossRef] [Green Version]
- Koshkin, V.; Wang, X.; Scherer, P.E.; Chan, C.B.; Wheeler, M.B. Mitochondrial functional state in clonal pancreatic beta-cells exposed to free fatty acids. J. Biol. Chem. 2003, 278, 19709–19715. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Solaini, G.; Baracca, A.; Lenaz, G.; Sgarbi, G. Hypoxia and mitochondrial oxidative metabolism. Biochim. Biophys. Acta 2010, 1797, 1171–1177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gerber, P.A.; Rutter, G.A. The Role of Oxidative Stress and Hypoxia in Pancreatic Beta-Cell Dysfunction in Diabetes Mellitus. Antioxid. Redox Signal. 2017, 26, 501–518. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hasnain, S.Z.; Prins, J.B.; McGuckin, M.A. Oxidative and endoplasmic reticulum stress in β-cell dysfunction in diabetes. J. Mol. Endocrinol. 2016, 56, R33–R54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cao, S.S.; Kaufman, R.J. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid. Redox Signal. 2014, 21, 396–413. [Google Scholar] [CrossRef] [PubMed]
- Freedman, M.S.; Bar-Or, A.; Atkins, H.L.; Karussis, D.; Frassoni, F.; Lazarus, H.; Scolding, N.; Slavin, S.; Le Blanc, K.; Uccelli, A.; et al. The therapeutic potential of mesenchymal stem cell transplantation as a treatment for multiple sclerosis: Consensus report of the International MSCT Study Group. Mult. Scler. 2010, 16, 503–510. [Google Scholar] [CrossRef]
- Newsholme, P.; Keane, D.; Welters, H.J.; Morgan, N.G. Life and death decisions of the pancreatic beta-cell: The role of fatty acids. Clin. Sci. 2007, 112, 27–42. [Google Scholar] [CrossRef] [Green Version]
- Kruman, I.; Guo, Q.; Mattson, M.P. Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. J. Neurosci. Res. 1998, 51, 293–308. [Google Scholar] [CrossRef]
- Yu, J.H.; Kim, K.H.; Kim, H. Role of NADPH oxidase and calcium in cerulein-induced apoptosis: Involvement of apoptosis-inducing factor. Ann. N. Y. Acad. Sci. 2006, 1090, 292–297. [Google Scholar] [CrossRef]
- Evans, J.L.; Goldfine, I.D.; Maddux, B.A.; Grodsky, G.M. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 2003, 52, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Newsholme, P.; Cruzat, V.F.; Keane, K.N.; Carlessi, R.; de Bittencourt, P.I.H. Molecular mechanisms of ROS production and oxidative stress in diabetes. Biochem. J. 2016, 473, 4527–4550. [Google Scholar] [CrossRef] [PubMed]
- Keane, K.N.; Cruzat, V.F.; Carlessi, R.; de Bittencourt, P.I.H.; Newsholme, P. Molecular Events Linking Oxidative Stress and Inflammation to Insulin Resistance and β-Cell Dysfunction. Oxid. Med. Cell. Longev. 2015, 2015, 181643. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Newsholme, P.; Rebelato, E.; Abdulkader, F.; Krause, M.; Carpinelli, A.; Curi, R. Reactive oxygen and nitrogen species generation, antioxidant defenses, and β-cell function: A critical role for amino acids. J. Endocrinol. 2012, 214, 11–20. [Google Scholar] [CrossRef] [PubMed]
- Ohlsson, H.; Karlsson, K.; Edlund, T. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J. 1993, 12, 4251–4259. [Google Scholar] [CrossRef] [PubMed]
- Kawamori, D.; Kajimoto, Y.; Kaneto, H.; Umayahara, Y.; Fujitani, Y.; Miyatsuka, T.; Watada, H.; Leibiger, I.B.; Yamasaki, Y.; Hori, M. Oxidative stress induces nucleo-cytoplasmic translocation of pancreatic transcription factor PDX-1 through activation of c-Jun NH(2)-terminal kinase. Diabetes 2003, 52, 2896–2904. [Google Scholar] [CrossRef] [Green Version]
- Kawamori, D.; Kaneto, H.; Nakatani, Y.; Matsuoka, T.-A.; Matsuhisa, M.; Hori, M.; Yamasaki, Y. The forkhead transcription factor Foxo1 bridges the JNK pathway and the transcription factor PDX-1 through its intracellular translocation. J. Biol. Chem. 2006, 281, 1091–1098. [Google Scholar] [CrossRef] [Green Version]
- Brownlee, M. A radical explanation for glucose-induced beta cell dysfunction. J. Clin. Investig. 2003, 112, 1788–1790. [Google Scholar] [CrossRef]
- Maechler, P.; Jornot, L.; Wollheim, C.B. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J. Biol. Chem. 1999, 274, 27905–27913. [Google Scholar] [CrossRef] [Green Version]
- Drews, G.; Krämer, C.; Düfer, M.; Krippeit-Drews, P. Contrasting effects of alloxan on islets and single mouse pancreatic beta-cells. Biochem. J. 2000, 352 Pt 2, 389–397. [Google Scholar] [CrossRef]
- Drews, G.; Krippeit-Drews, P.; Düfer, M. Oxidative stress and beta-cell dysfunction. Pflugers Arch. 2010, 460, 703–718. [Google Scholar] [CrossRef]
- Tiwari, B.K.; Pandey, K.B.; Abidi, A.B.; Rizvi, S.I. Markers of Oxidative Stress during Diabetes Mellitus. J. Biomark. 2013, 2013, 378790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Phillips, M.; Cataneo, R.N.; Cheema, T.; Greenberg, J. Increased breath biomarkers of oxidative stress in diabetes mellitus. Clin. Chim. Acta 2004, 344, 189–194. [Google Scholar] [CrossRef] [PubMed]
- Asmat, U.; Abad, K.; Ismail, K. Diabetes mellitus and oxidative stress-A concise review. Saudi Pharm. J. 2016, 24, 547–553. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Asfandiyarova, N.; Kolcheva, N.; Ryazantsev, I.; Ryazantsev, V. Risk factors for stroke in type 2 diabetes mellitus. Diabetes Vasc. Dis. Res. 2006, 3, 57–60. [Google Scholar] [CrossRef] [PubMed]
- Poy, M.N.; Eliasson, L.; Krutzfeldt, J.; Kuwajima, S.; Ma, X.; Macdonald, P.E.; Pfeffer, S.; Tuschl, T.; Rajewsky, N.; Rorsman, P.; et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004, 432, 226–230. [Google Scholar] [CrossRef] [PubMed]
- Shantikumar, S.; Caporali, A.; Emanueli, C. Role of microRNAs in diabetes and its cardiovascular complications. Cardiovasc. Res. 2012, 93, 583–593. [Google Scholar] [CrossRef] [Green Version]
- Lenzen, S. Chemistry and biology of reactive species with special reference to the antioxidativedefence status in pancreatic β-cells. Biochim. Biophys. Acta Gen. Subj. 2017, 1861, 1929–1942. [Google Scholar] [CrossRef]
- Qadir, M.M.F.; Klein, D.; Álvarez-Cubela, S.; Domínguez-Bendala, J.; Pastori, R.L. The Role of MicroRNAs in Diabetes-Related Oxidative Stress. Int. J. Mol. Sci. 2019, 20, 5423. [Google Scholar] [CrossRef] [Green Version]
- Robertson, R.P. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J. Biol. Chem. 2004, 279, 42351–42354. [Google Scholar] [CrossRef] [Green Version]
- Gehrmann, W.; Elsner, M.; Lenzen, S. Role of metabolically generated reactive oxygen species for lipotoxicity in pancreatic β-cells. Diabetes Obes. Metab. 2010, 12 (Suppl. 2), 149–158. [Google Scholar] [CrossRef]
- Ozcan, U.; Yilmaz, E.; Ozcan, L.; Furuhashi, M.; Vaillancourt, E.; Smith, R.O.; Görgün, C.Z.; Hotamisligil, G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313, 1137–1140. [Google Scholar] [CrossRef] [Green Version]
- Chu, K.; Tsai, M.-J. Neuronatin, a downstream target of BETA2/NeuroD1 in the pancreas, is involved in glucose-mediated insulin secretion. Diabetes 2005, 54, 1064–1073. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodríguez-Comas, J.; Moreno-Asso, A.; Moreno-Vedia, J.; Martín, M.; Castaño, C.; Marzà-Florensa, A.; Bofill-De Ros, X.; Mir-Coll, J.; Montané, J.; Fillat, C.; et al. Stress-Induced MicroRNA-708 Impairs β-Cell Function and Growth. Diabetes 2017, 66, 3029–3040. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lovis, P.; Roggli, E.; Laybutt, D.R.; Gattesco, S.; Yang, J.-Y.; Widmann, C.; Abderrahmani, A.; Regazzi, R. Alterations in microRNA expression contribute to fatty acid-induced pancreatic beta-cell dysfunction. Diabetes 2008, 57, 2728–2736. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matsuo, Y.; Tanaka, M.; Yamakage, H.; Sasaki, Y.; Muranaka, K.; Hata, H.; Ikai, I.; Shimatsu, A.; Inoue, M.; Chun, T.-H.; et al. Thrombospondin 1 as a novel biological marker of obesity and metabolic syndrome. Metab. Clin. Exp. 2015, 64, 1490–1499. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.; Dong, J.; Ren, B. MicroRNA-182-5p contributes to the protective effects of thrombospondin 1 against lipotoxicity in INS-1 cells. Exp. Ther. Med. 2018, 16, 5272–5279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.; Liu, H.; Li, Q. Glucagon-like peptide-1 effects lipotoxic oxidative stress by regulating the expression of microRNAs. Biochem. Biophys. Res. Commun. 2017, 482, 1462–1468. [Google Scholar] [CrossRef] [PubMed]
- Belgardt, B.-F.; Ahmed, K.; Spranger, M.; Latreille, M.; Denzler, R.; Kondratiuk, N.; von Meyenn, F.; Villena, F.N.; Herrmanns, K.; Bosco, D.; et al. The microRNA-200 family regulates pancreatic beta cell survival in type 2 diabetes. Nat. Med. 2015, 21, 619–627. [Google Scholar] [CrossRef] [Green Version]
- Chen, D.-L.; Yang, K.-Y. Berberine Alleviates Oxidative Stress in Islets of Diabetic Mice by Inhibiting miR-106b Expression and Up-Regulating SIRT1. J. Cell Biochem. 2017, 118, 4349–4357. [Google Scholar] [CrossRef]
- Dai, F.; Liu, T.; Zheng, S.; Liu, Q.; Yang, C.; Zhou, J.; Chen, Y.; Sheyhidin, I.; Lu, X. MiR-106b promotes migration and invasion through enhancing EMT via downregulation of Smad 7 in Kazakh’s esophageal squamous cell carcinoma. Tumour Biol. 2016, 37, 14595–14604. [Google Scholar] [CrossRef]
- Zhang, F.; Li, Z.-L.; Xu, X.-M.; Hu, Y.; Yao, J.-H.; Xu, W.; Jing, H.-R.; Wang, S.; Ning, S.-L.; Tian, X.-F. Protective effects of icariin-mediated SIRT1/FOXO3 signaling pathway on intestinal ischemia/reperfusion-induced acute lung injury. Mol. Med. Rep. 2015, 11, 269–276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fu, Y.; Zhang, Y.; Wang, Z.; Wang, L.; Wei, X.; Zhang, B.; Wen, Z.; Fang, H.; Pang, Q.; Yi, F. Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy. Am. J. Nephrol. 2010, 32, 581–589. [Google Scholar] [CrossRef] [PubMed]
- Vasa-Nicotera, M.; Chen, H.; Tucci, P.; Yang, A.L.; Saintigny, G.; Menghini, R.; Mahè, C.; Agostini, M.; Knight, R.A.; Melino, G.; et al. miR-146a is modulated in human endothelial cell with aging. Atherosclerosis 2011, 217, 326–330. [Google Scholar] [CrossRef] [PubMed]
- Feng, B.; Chen, S.; McArthur, K.; Wu, Y.; Sen, S.; Ding, Q.; Feldman, R.D.; Chakrabarti, S. miR-146a-Mediated extracellular matrix protein production in chronic diabetes complications. Diabetes 2011, 60, 2975–2984. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muratsu-Ikeda, S.; Nangaku, M.; Ikeda, Y.; Tanaka, T.; Wada, T.; Inagi, R. Downregulation of miR-205 modulates cell susceptibility to oxidative and endoplasmic reticulum stresses in renal tubular cells. PLoS ONE 2012, 7, e41462. [Google Scholar] [CrossRef] [Green Version]
- Kato, M.; Putta, S.; Wang, M.; Yuan, H.; Lanting, L.; Nair, I.; Gunn, A.; Nakagawa, Y.; Shimano, H.; Todorov, I.; et al. TGF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat. Cell Biol. 2009, 11, 881–889. [Google Scholar] [CrossRef] [Green Version]
- Beckman, J.D.; Chen, C.; Nguyen, J.; Thayanithy, V.; Subramanian, S.; Steer, C.J.; Vercellotti, G.M. Regulation of heme oxygenase-1 protein expression by miR-377 in combination with miR-217. J. Biol. Chem. 2011, 286, 3194–3202. [Google Scholar] [CrossRef] [Green Version]
- La Sala, L.; Cattaneo, M.; De Nigris, V.; Pujadas, G.; Testa, R.; Bonfigli, A.R.; Genovese, S.; Ceriello, A. Oscillating glucose induces microRNA-185 and impairs an efficient antioxidant response in human endothelial cells. Cardiovasc. Diabetol. 2016, 15, 71. [Google Scholar] [CrossRef] [Green Version]
- Yu, M.; Liu, Y.; Zhang, B.; Shi, Y.; Cui, L.; Zhao, X. Inhibiting microRNA-144 abates oxidative stress and reduces apoptosis in hearts of streptozotocin-induced diabetic mice. Cardiovasc. Pathol. 2015, 24, 375–381. [Google Scholar] [CrossRef]
- Yang, S.; Fei, X.; Lu, Y.; Xu, B.; Ma, Y.; Wan, H. miRNA-214 suppresses oxidative stress in diabetic nephropathy via the ROS/Akt/mTOR signaling pathway and uncoupling protein 2. Exp. Ther. Med. 2019, 17, 3530–3538. [Google Scholar] [CrossRef] [Green Version]
- La Sala, L.; Mrakic-Sposta, S.; Micheloni, S.; Prattichizzo, F.; Ceriello, A. Glucose-sensing microRNA-21 disrupts ROS homeostasis and impairs antioxidant responses in cellular glucose variability. Cardiovasc. Diabetol. 2018, 17, 105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- La Sala, L.; Mrakic-Sposta, S.; Tagliabue, E.; Prattichizzo, F.; Micheloni, S.; Sangalli, E.; Specchia, C.; Uccellatore, A.C.; Lupini, S.; Spinetti, G.; et al. Circulating microRNA-21 is an early predictor of ROS-mediated damage in subjects with high risk of developing diabetes and in drug-naïve T2D. Cardiovasc. Diabetol. 2019, 18, 18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tang, Q.; Len, Q.; Liu, Z.; Wang, W. Overexpression of miR-22 attenuates oxidative stress injury in diabetic cardiomyopathy via Sirt 1. Cardiovasc. Ther. 2018, 36, e12318. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gou, L.; Zhao, L.; Song, W.; Wang, L.; Liu, J.; Zhang, H.; Huang, Y.; Lau, C.W.; Yao, X.; Tian, X.Y.; et al. Inhibition of miR-92a Suppresses Oxidative Stress and Improves Endothelial Function by UpregulatingHeme Oxygenase-1 in db/db Mice. Antioxid. Redox Signal. 2018, 28, 358–370. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kamalden, T.A.; Macgregor-Das, A.M.; Kannan, S.M.; Dunkerly-Eyring, B.; Khaliddin, N.; Xu, Z.; Fusco, A.P.; Yazib, S.A.; Chow, R.C.; Duh, E.J.; et al. Exosomal MicroRNA-15a Transfer from the Pancreas Augments Diabetic Complications by Inducing Oxidative Stress. Antioxid. Redox Signal. 2017, 27, 913–930. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Zhang, J.; Chen, X.; Yang, Y.; Wang, F.; Li, W.; Awuti, M.; Sun, Y.; Lian, C.; Li, Z.; et al. miR-365 promotes diabetic retinopathy through inhibiting Timp3 and increasing oxidative stress. Exp. Eye Res. 2018, 168, 89–99. [Google Scholar] [CrossRef] [PubMed]
- Togliatto, G.; Trombetta, A.; Dentelli, P.; Gallo, S.; Rosso, A.; Cotogni, P.; Granata, R.; Falcioni, R.; Delale, T.; Ghigo, E.; et al. Unacylated ghrelin induces oxidative stress resistance in a glucose intolerance and peripheral artery disease mouse model by restoring endothelial cell miR-126 expression. Diabetes 2015, 64, 1370–1382. [Google Scholar] [CrossRef] [Green Version]
- Li, Q.; Kim, Y.-R.; Vikram, A.; Kumar, S.; Kassan, M.; Gabani, M.; Lee, S.K.; Jacobs, J.S.; Irani, K. P66Shc-Induced MicroRNA-34a Causes Diabetic Endothelial Dysfunction by Downregulating Sirtuin1. Arterioscler. Thromb. Vasc. Biol. 2016, 36, 2394–2403. [Google Scholar] [CrossRef] [Green Version]
- Giza, D.E.; Vasilescu, C.; Calin, G.A. Key principles of miRNA involvement in human diseases. Discoveries 2014, 2, e34. [Google Scholar] [CrossRef]
- Fasoulakis, Z.; Daskalakis, G.; Diakosavvas, M.; Papapanagiotou, I.; Theodora, M.; Bourazan, A.; Alatzidou, D.; Pagkalos, A.; Kontomanolis, N.E. MicroRNAs determining carcinogenesis by regulating oncogenes and tumor suppressor genes during cell cycle. Microrna 2019. [Google Scholar] [CrossRef]
- Li, J.; Zhong, Y.; Cai, S.; Zhou, P.; Yao, L. MicroRNA expression profiling in the colorectal normal-adenoma-carcinoma transition. Oncol. Lett. 2019, 18, 2013–2018. [Google Scholar] [CrossRef]
- Mirzaei, S.; Baghaei, K.; Parivar, K.; Hashemi, M.; AsadzadehAghdaei, H. The expression level changes of microRNAs 200a/205 in the development of invasive properties in gastric cancer cells through epithelial-mesenchymal transition. Eur. J. Pharmacol. 2019, 857, 172426. [Google Scholar] [CrossRef] [PubMed]
- Peng, B.; Chen, Y.; Leong, K.W. MicroRNA delivery for regenerative medicine. Adv. Drug Deliv. Rev. 2015, 88, 108–122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Z. The guideline of the design and validation of MiRNA mimics. Methods Mol. Biol. 2011, 676, 211–223. [Google Scholar] [PubMed]
- Wang, Z. Multi-miRNA Hairpins and Multi-miRNA Mimics Technologies. In MicroRNA Interference Technologies; Springer: Berlin/Heidelberg, Germany, 2009; pp. 101–110. [Google Scholar]
- Ebert, M.S.; Sharp, P.A. MicroRNA sponges: Progress and possibilities. RNA 2010, 16, 2043–2050. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, Q.-H.; Wang, M.-B. Molecular Functions of Long Non-Coding RNAs in Plants. Genes 2012, 3, 176–190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, D.-L.; Ju, H.-Q.; Lu, Y.-X.; Chen, L.-Z.; Zeng, Z.-L.; Zhang, D.-S.; Luo, H.-Y.; Wang, F.; Qiu, M.-Z.; Wang, D.-S.; et al. Long non-coding RNA XIST regulates gastric cancer progression by acting as a molecular sponge of miR-101 to modulate EZH2 expression. J. Exp. Clin. Cancer Res. 2016, 35, 142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ebert, M.S.; Neilson, J.R.; Sharp, P.A. MicroRNA sponges: Competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 2007, 4, 721–726. [Google Scholar] [CrossRef]
- Guo, J.U.; Agarwal, V.; Guo, H.; Bartel, D.P. Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 2014, 15, 409. [Google Scholar] [CrossRef]
- Dias, N.; Stein, C.A. Antisense oligonucleotides: Basic concepts and mechanisms. Mol. Cancer Ther. 2002, 1, 347–355. [Google Scholar]
- Krützfeldt, J.; Kuwajima, S.; Braich, R.; Rajeev, K.G.; Pena, J.; Tuschl, T.; Manoharan, M.; Stoffel, M. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res. 2007, 35, 2885–2892. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lennox, K.A.; Behlke, M.A. A direct comparison of anti-microRNA oligonucleotide potency. Pharm. Res. 2010, 27, 1788–1799. [Google Scholar] [CrossRef] [PubMed]
- Shen, W.; De Hoyos, C.L.; Migawa, M.T.; Vickers, T.A.; Sun, H.; Low, A.; Bell, T.A.; Rahdar, M.; Mukhopadhyay, S.; Hart, C.E.; et al. Chemical modification of PS-ASO therapeutics reduces cellular protein-binding and improves the therapeutic index. Nat. Biotechnol. 2019, 37, 640–650. [Google Scholar] [CrossRef] [PubMed]
- Jing, Z.; Qi, R.; Thibonnier, M.; Ren, P. Molecular Dynamics Study of the Hybridization between RNA and Modified Oligonucleotides. J. Chem. Theory Comput. 2019, 15, 11. [Google Scholar] [CrossRef] [PubMed]
- Gebert, L.F.R.; Rebhan, M.A.E.; Crivelli, S.E.M.; Denzler, R.; Stoffel, M.; Hall, J. Miravirsen (SPC3649) can inhibit the biogenesis of miR-122. Nucleic Acids Res. 2014, 42, 609–621. [Google Scholar] [CrossRef] [Green Version]
- Lindow, M.; Kauppinen, S. Discovering the first microRNA-targeted drug. J. Cell Biol. 2012, 199, 407–412. [Google Scholar] [CrossRef]
- Conrad, K.D.; Giering, F.; Erfurth, C.; Neumann, A.; Fehr, C.; Meister, G.; Niepmann, M. MicroRNA-122 dependent binding of Ago2 protein to hepatitis C virus RNA is associated with enhanced RNA stability and translation stimulation. PLoS ONE 2013, 8, e56272. [Google Scholar] [CrossRef] [Green Version]
- Norman, K.L.; Sarnow, P. Modulation of hepatitis C virus RNA abundance and the isoprenoid biosynthesis pathway by microRNA miR-122 involves distinct mechanisms. J. Virol. 2010, 84, 666–670. [Google Scholar] [CrossRef] [Green Version]
- Janssen, H.L.A.; Reesink, H.W.; Lawitz, E.J.; Zeuzem, S.; Rodriguez-Torres, M.; Patel, K.; van der Meer, A.J.; Patick, A.K.; Chen, A.; Zhou, Y.; et al. Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 2013, 368, 1685–1694. [Google Scholar] [CrossRef] [Green Version]
- Tonga, G.Y.; Moyano, D.F.; Kim, C.S.; Rotello, V.M. Inorganic nanoparticles for therapeutic delivery: Trials, tribulations and promise. Curr. Opin. Colloid Interface Sci. 2014, 19, 49–55. [Google Scholar] [CrossRef] [Green Version]
- Chaudhary, V.; Jangra, S.; Yadav, N.R. Nanotechnology based approaches for detection and delivery of microRNA in healthcare and crop protection. J. Nanobiotechnol. 2018, 16, 40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nelson, B.C.; Johnson, M.E.; Walker, M.L.; Riley, K.R.; Sims, C.M. Antioxidant cerium oxide nanoparticles in biology and medicine. Antioxidants 2016, 5, 15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kong, F.-Y.; Zhang, J.-W.; Li, R.-F.; Wang, Z.-X.; Wang, W.-J.; Wang, W. Unique roles of gold nanoparticles in drug delivery, targeting and imaging applications. Molecules 2017, 22, 1445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ding, Y.; Jiang, Z.; Saha, K.; Kim, C.S.; Kim, S.T.; Landis, R.F.; Rotello, V.M. Gold nanoparticles for nucleic acid delivery. Mol. Ther. 2014, 22, 1075–1083. [Google Scholar] [CrossRef] [Green Version]
- Freitas de Freitas, L.; Varca, G.H.C.; Dos Santos Batista, J.G.; BenévoloLugão, A. An overview of the synthesis of gold nanoparticles using radiation technologies. Nanomaterials 2018, 8, 939. [Google Scholar] [CrossRef] [Green Version]
- Jiang, Y.; Zhao, H.; Zhu, N.; Lin, Y.; Yu, P.; Mao, L. A simple assay for direct colorimetric visualization of trinitrotoluene at picomolar levels using gold nanoparticles. Angew. Chem. Int. Ed. Engl. 2008, 47, 8601–8604. [Google Scholar] [CrossRef]
- Brink, G.; Schmitt, L.; Tampé, R.; Sackmann, E. Self assembly of covalently anchored phospholipid supported membranes by use of DODA-Suc-NHS-lipids. Biochim. Biophys. Acta 1994, 1196, 227–230. [Google Scholar] [CrossRef]
- Kang, J.; Zhang, Y.; Li, X.; Miao, L.; Wu, A. A Rapid Colorimetric Sensor of Clenbuterol Based on Cysteamine-Modified Gold Nanoparticles. ACS Appl. Mater. Interfaces 2016, 8, 1–5. [Google Scholar] [CrossRef]
- Sábio, R.M.; Meneguin, A.B.; Ribeiro, T.C.; Silva, R.R.; Chorilli, M. New insights towards mesoporous silica nanoparticles as a technological platform for chemotherapeutic drugs delivery. Int. J. Pharm. 2019, 564, 379–409. [Google Scholar] [CrossRef]
- Palanikumar, L.; Choi, E.S.; Oh, J.Y.; Park, S.A.; Choi, H.; Kim, K.; Kim, C.; Ryu, J.-H. Importance of Encapsulation Stability of Nanocarriers with High Drug Loading Capacity for Increasing in Vivo Therapeutic Efficacy. Biomacromolecules 2018, 19, 3030–3039. [Google Scholar] [CrossRef]
- Vallet-Regí, M.; Colilla, M.; Izquierdo-Barba, I.; Manzano, M. Mesoporous silica nanoparticles for drug delivery: Current insights. Molecules 2017, 23, 47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Narayan, R.; Nayak, U.Y.; Raichur, A.M.; Garg, S. Mesoporous silica nanoparticles: A comprehensive review on synthesis and recent advances. Pharmaceutics 2018, 10, 118. [Google Scholar] [CrossRef] [Green Version]
- Tivnan, A.; Orr, W.S.; Gubala, V.; Nooney, R.; Williams, D.E.; McDonagh, C.; Prenter, S.; Harvey, H.; Domingo-Fernández, R.; Bray, I.M.; et al. Inhibition of neuroblastoma tumor growth by targeted delivery of microRNA-34a using anti-disialoganglioside GD2 coated nanoparticles. PLoS ONE 2012, 7, e38129. [Google Scholar] [CrossRef] [PubMed]
- Celardo, I.; Pedersen, J.Z.; Traversa, E.; Ghibelli, L. Pharmacological potential of cerium oxide nanoparticles. Nanoscale 2011, 3, 1411–1420. [Google Scholar] [CrossRef] [PubMed]
- Xu, C.; Lin, Y.; Wang, J.; Wu, L.; Wei, W.; Ren, J.; Qu, X. Nanoceria-triggered synergetic drug release based on CeO(2)-capped mesoporous silica host-guest interactions and switchable enzymatic activity and cellular effects of CeO(2). Adv. Healthc. Mater. 2013, 2, 1591–1599. [Google Scholar] [CrossRef] [PubMed]
- Karakoti, A.S.; Tsigkou, O.; Yue, S.; Lee, P.D.; Stevens, M.M.; Jones, J.R.; Seal, S. Rare earth oxides as nanoadditives in 3-D nanocomposite scaffolds for bone regeneration. J. Mater. Chem. 2010, 20, 8912. [Google Scholar] [CrossRef]
- Kwon, H.J.; Cha, M.-Y.; Kim, D.; Kim, D.K.; Soh, M.; Shin, K.; Hyeon, T.; Mook-Jung, I. Mitochondria-Targeting Ceria Nanoparticles as Antioxidants for Alzheimer’s Disease. ACS Nano 2016, 10, 2860–2870. [Google Scholar] [CrossRef]
- Dhall, A.; Self, W. Cerium oxide nanoparticles: A brief review of their synthesis methods and biomedical applications. Antioxidants 2018, 7, 97. [Google Scholar] [CrossRef] [Green Version]
- Zgheib, C.; Hilton, S.A.; Dewberry, L.C.; Hodges, M.M.; Ghatak, S.; Xu, J.; Singh, S.; Roy, S.; Sen, C.K.; Seal, S.; et al. Use of Cerium Oxide Nanoparticles Conjugated with MicroRNA-146a to Correct the Diabetic Wound Healing Impairment. J. Am. Coll. Surg. 2019, 228, 107–115. [Google Scholar] [CrossRef]
- Geim, A.K.; Novoselov, K.S. The rise of graphene. Nat. Mater. 2007, 6, 183–191. [Google Scholar] [CrossRef]
- Sun, X.; Liu, Z.; Welsher, K.; Robinson, J.T.; Goodwin, A.; Zaric, S.; Dai, H. Nano-Graphene Oxide for Cellular Imaging and Drug Delivery. Nano Res. 2008, 1, 203–212. [Google Scholar] [CrossRef] [Green Version]
- Mody, V.V.; Siwale, R.; Singh, A.; Mody, H.R. Introduction to metallic nanoparticles. J. Pharm. Bioallied Sci. 2010, 2, 282–289. [Google Scholar] [CrossRef]
- Fu, P.P.; Xia, Q.; Hwang, H.-M.; Ray, P.C.; Yu, H. Mechanisms of nanotoxicity: Generation of reactive oxygen species. J. Food Drug Anal. 2014, 22, 64–75. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Liu, S.; Jia, L.; Chu, F.; Zhou, Y.; He, Z.; Guo, M.; Chen, C.; Xu, L. Nanostructured lipid carriers for MicroRNA delivery in tumor gene therapy. Cancer Cell Int. 2018, 18, 101. [Google Scholar] [CrossRef]
- Panahi, Y.; Farshbaf, M.; Mohammadhosseini, M.; Mirahadi, M.; Khalilov, R.; Saghfi, S.; Akbarzadeh, A. Recent advances on liposomal nanoparticles: Synthesis, characterization and biomedical applications. Artif. Cells Nanomed. Biotechnol. 2017, 45, 788–799. [Google Scholar] [CrossRef] [Green Version]
- Anwer, K.; Meaney, C.; Kao, G.; Hussain, N.; Shelvin, R.; Earls, R.M.; Leonard, P.; Quezada, A.; Rolland, A.P.; Sullivan, S.M. Cationic lipid-based delivery system for systemic cancer gene therapy. Cancer Gene Ther. 2000, 7, 1156–1164. [Google Scholar] [CrossRef] [Green Version]
- Pramanik, D.; Campbell, N.R.; Karikari, C.; Chivukula, R.; Kent, O.A.; Mendell, J.T.; Maitra, A. Restitution of tumor suppressor microRNAs using a systemic nanovector inhibits pancreatic cancer growth in mice. Mol. Cancer Ther. 2011, 10, 1470–1480. [Google Scholar] [CrossRef] [Green Version]
- Beg, M.S.; Brenner, A.J.; Sachdev, J.; Borad, M.; Kang, Y.-K.; Stoudemire, J.; Smith, S.; Bader, A.G.; Kim, S.; Hong, D.S. Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Investig. New Drugs 2017, 35, 180–188. [Google Scholar] [CrossRef]
- Yamakuchi, M.; Ferlito, M.; Lowenstein, C.J. miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. USA 2008, 105, 13421–13426. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Huang, Q.; Zeng, Z.; Wu, J.; Zhang, Y.; Chen, Z. Sirt1 inhibits oxidative stress in vascular endothelial cells. Oxid. Med. Cell. Longev. 2017, 2017, 7543973. [Google Scholar] [CrossRef] [Green Version]
- Fomison-Nurse, I.; Saw, E.E.L.; Gandhi, S.; Munasinghe, P.E.; Van Hout, I.; Williams, M.J.A.; Galvin, I.; Bunton, R.; Davis, P.; Cameron, V.; et al. Diabetes induces the activation of pro-ageing miR-34a in the heart, but has differential effects on cardiomyocytes and cardiac progenitor cells. Cell Death Differ. 2018, 25, 1336–1349. [Google Scholar] [CrossRef] [Green Version]
- Bernardo, B.C.; Gao, X.-M.; Tham, Y.K.; Kiriazis, H.; Winbanks, C.E.; Ooi, J.Y.Y.; Boey, E.J.H.; Obad, S.; Kauppinen, S.; Gregorevic, P.; et al. Silencing of miR-34a attenuates cardiac dysfunction in a setting of moderate, but not severe, hypertrophic cardiomyopathy. PLoS ONE 2014, 9, e90337. [Google Scholar] [CrossRef]
- Palmerston Mendes, L.; Pan, J.; Torchilin, V.P. Dendrimers as nanocarriers for nucleic acid and drug delivery in cancer therapy. Molecules 2017, 22, 1401. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Zhao, X.; Guo, C.; Ren, D.; Zhao, Y.; Xiao, W.; Jiao, W. Aptamer-DendrimerBioconjugates for Targeted Delivery of miR-34a Expressing Plasmid and Antitumor Effects in Non-Small Cell Lung Cancer Cells. PLoS ONE 2015, 10, e0139136. [Google Scholar]
- Santos-Carballal, B.; Aaldering, L.J.; Ritzefeld, M.; Pereira, S.; Sewald, N.; Moerschbacher, B.M.; Götte, M.; Goycoolea, F.M. Physicochemical and biological characterization of chitosan-microRNA nanocomplexes for gene delivery to MCF-7 breast cancer cells. Sci. Rep. 2015, 5, 13567. [Google Scholar] [CrossRef]
- Mohammed, M.A.; Syeda, J.T.M.; Wasan, K.M.; Wasan, E.K. An Overview of Chitosan Nanoparticles and Its Application in Non-Parenteral Drug Delivery. Pharmaceutics 2017, 9, 53. [Google Scholar] [CrossRef] [Green Version]
- Gaur, S.; Wen, Y.; Song, J.H.; Parikh, N.U.; Mangala, L.S.; Blessing, A.M.; Ivan, C.; Wu, S.Y.; Varkaris, A.; Shi, Y.; et al. Chitosan nanoparticle-mediated delivery of miRNA-34a decreases prostate tumor growth in the bone and its expression induces non-canonical autophagy. Oncotarget 2015, 6, 29161–29177. [Google Scholar] [CrossRef] [Green Version]
- Keefe, A.D.; Pai, S.; Ellington, A. Aptamers as therapeutics. Nat. Rev. Drug Discov. 2010, 9, 537–550. [Google Scholar] [CrossRef]
- Gelinas, A.D.; Davies, D.R.; Janjic, N. Embracing proteins: Structural themes in aptamer-protein complexes. Curr. Opin. Struct. Biol. 2016, 36, 122–132. [Google Scholar] [CrossRef] [Green Version]
- Hermann, T.; Patel, D.J. Adaptive recognition by nucleic acid aptamers. Science 2000, 287, 820–825. [Google Scholar] [CrossRef] [Green Version]
- Gold, L. Oligonucleotides as research, diagnostic, and therapeutic agents. J. Biol. Chem. 1995, 270, 13581–13584. [Google Scholar] [CrossRef] [Green Version]
- Zhuo, Z.; Yu, Y.; Wang, M.; Li, J.; Zhang, Z.; Liu, J.; Wu, X.; Lu, A.; Zhang, G.; Zhang, B. Recent advances in SELEX technology and aptamer applications in biomedicine. Int. J. Mol. Sci. 2017, 18, 2142. [Google Scholar] [CrossRef] [Green Version]
- Blind, M.; Blank, M. Aptamer selection technology and recent advances. Mol. Ther. Nucleic Acids 2015, 4, e223. [Google Scholar] [CrossRef]
- Urak, K.T.; Shore, S.; Rockey, W.M.; Chen, S.-J.; McCaffrey, A.P.; Giangrande, P.H. In vitro RNA SELEX for the generation of chemically-optimized therapeutic RNA drugs. Methods 2016, 103, 167–174. [Google Scholar] [CrossRef] [Green Version]
- Zhu, Q.; Liu, G.; Kai, M. DNA aptamers in the diagnosis and treatment of human diseases. Molecules 2015, 20, 20979–20997. [Google Scholar] [CrossRef]
- Shu, Y.; Pi, F.; Sharma, A.; Rajabi, M.; Haque, F.; Shu, D.; Leggas, M.; Evers, B.M.; Guo, P. Stable RNA nanoparticles as potential new generation drugs for cancer therapy. Adv. Drug Deliv. Rev. 2014, 66, 74–89. [Google Scholar] [CrossRef] [Green Version]
- Lipi, F.; Chen, S.; Chakravarthy, M.; Rakesh, S.; Veedu, R.N. In vitro evolution of chemically-modified nucleic acid aptamers: Pros and cons, and comprehensive selection strategies. RNA Biol. 2016, 13, 1232–1245. [Google Scholar] [CrossRef] [Green Version]
- Hirao, I.; Kimoto, M.; Mitsui, T.; Fujiwara, T.; Kawai, R.; Sato, A.; Harada, Y.; Yokoyama, S. An unnatural hydrophobic base pair system: Site-specific incorporation of nucleotide analogs into DNA and RNA. Nat. Methods 2006, 3, 729–735. [Google Scholar] [CrossRef]
- Wang, T.; Chen, C.; Larcher, L.M.; Barrero, R.A.; Veedu, R.N. Three decades of nucleic acid aptamer technologies: Lessons learned, progress and opportunities on aptamer development. Biotechnol. Adv. 2019, 37, 28–50. [Google Scholar] [CrossRef]
- Zhou, J.; Rossi, J.J. Cell-type-specific, Aptamer-functionalized Agents for Targeted Disease Therapy. Mol. Ther. Nucleic Acids 2014, 3, e169. [Google Scholar] [CrossRef]
- Li, C.-J.; Cheng, P.; Liang, M.-K.; Chen, Y.-S.; Lu, Q.; Wang, J.-Y.; Xia, Z.-Y.; Zhou, H.-D.; Cao, X.; Xie, H.; et al. MicroRNA-188 regulates age-related switch between osteoblast and adipocyte differentiation. J. Clin. Investig. 2015, 125, 1509–1522. [Google Scholar] [CrossRef] [Green Version]
- Iaboni, M.; Russo, V.; Fontanella, R.; Roscigno, G.; Fiore, D.; Donnarumma, E.; Esposito, C.L.; Quintavalle, C.; Giangrande, P.H.; de Franciscis, V.; et al. Aptamer-miRNA-212 Conjugate Sensitizes NSCLC Cells to TRAIL. Mol. Ther. Nucleic Acids 2016, 5, e289. [Google Scholar] [CrossRef] [Green Version]
- Seo, Y.-E.; Suh, H.-W.; Bahal, R.; Josowitz, A.; Zhang, J.; Song, E.; Cui, J.; Noorbakhsh, S.; Jackson, C.; Bu, T.; et al. Nanoparticle-mediated intratumoral inhibition of miR-21 for improved survival in glioblastoma. Biomaterials 2019, 201, 87–98. [Google Scholar] [CrossRef]
- Malhotra, M.; Sekar, T.V.; Ananta, J.S.; Devulapally, R.; Afjei, R.; Babikir, H.A.; Paulmurugan, R.; Massoud, T.F. Targeted nanoparticle delivery of therapeutic antisense microRNAs presensitizesglioblastoma cells to lower effective doses of temozolomide in vitro and in a mouse model. Oncotarget 2018, 9, 21478–21494. [Google Scholar] [CrossRef] [Green Version]
- Jones Buie, J.N.; Zhou, Y.; Goodwin, A.J.; Cook, J.A.; Vournakis, J.; Demcheva, M.; Broome, A.-M.; Dixit, S.; Halushka, P.V.; Fan, H. Application of Deacetylated Poly-N-Acetyl Glucosamine Nanoparticles for the Delivery of miR-126 for the Treatment of Cecal Ligation and Puncture-Induced Sepsis. Inflammation 2019, 42, 170–184. [Google Scholar] [CrossRef]
- Fish, J.E.; Santoro, M.M.; Morton, S.U.; Yu, S.; Yeh, R.-F.; Wythe, J.D.; Ivey, K.N.; Bruneau, B.G.; Stainier, D.Y.R.; Srivastava, D. miR-126 regulates angiogenic signaling and vascular integrity. Dev. Cell 2008, 15, 272–284. [Google Scholar] [CrossRef] [Green Version]
- Luo, Q.; Feng, Y.; Xie, Y.; Shao, Y.; Wu, M.; Deng, X.; Yuan, W.-E.; Chen, Y.; Shi, X. Nanoparticle-microRNA-146a-5p polyplexes ameliorate diabetic peripheral neuropathy by modulating inflammation and apoptosis. Nanomedicine 2019, 17, 188–197. [Google Scholar] [CrossRef]
- King, G.L.; Loeken, M.R. Hyperglycemia-induced oxidative stress in diabetic complications. Histochem. Cell Biol. 2004, 122, 333–338. [Google Scholar] [CrossRef]
- Rolo, A.P.; Palmeira, C.M. Diabetes and mitochondrial function: Role of hyperglycemia and oxidative stress. Toxicol. Appl. Pharmacol. 2006, 212, 167–178. [Google Scholar] [CrossRef] [Green Version]
- Liang, Y.-Z.; Li, J.-J.-H.; Xiao, H.-B.; He, Y.; Zhang, L.; Yan, Y.-X. Identification of stress-related microRNA biomarkers in type 2 diabetes mellitus: A systematic review and meta-analysis. J. Diabetes 2018. [Google Scholar] [CrossRef] [Green Version]
MicroRNA | Cell/Tissue | Target Gene | Target GeneFunction | Disease or Dysfunction | Ref. |
---|---|---|---|---|---|
miR-708 ↑ | - Mouse pancreatic islets (ob/ob mice) - Min6 β-cell line; Ins1 β-cell line | Neuronatin↓ | Overexpression of Neuronatin restores β cell function under ER stress | T2D | [51,52,53] |
miR-34a ↑ | - Min6 β-cell line - Islets from C57/Bl6 KsJ db/db - Rat pancreatic islets | T2D | [9,54] | ||
miR-146 ↑ | - Min6 β-cell line - Islets from C57/Bl6 KsJ db/db - Rat pancreatic islets | T2D | [9,54] | ||
miR-182-5p ↓ | - Visceral and subcutaneous adipose tissue from human donors - Ins1 β-cell line | THBS-1 ↑ | Upregulation of THBS-1 protects β cells from lipotoxic damage | T2D | [55,56] |
miR-370 ↓ miR-33 ↓ | - Ins1 β-cell line - C57BL/6 mice HFD | T2D | [57] | ||
miR-200 family ↑ | - db/db mice - Min6 β-cell line | p58IPK/XIAP ↓ | Physiologic expression of p58IPK/XIAP protects the β cells from oxidative stress | T2D | [58] |
miR-106-b ↓ | - db/db mice - NIT-1 β-cell line | SIRT-1 ↑ | SIRT-1 upregulation leads the reduction of pro-apoptotic molecules expression through FoxO1 activation | T2D | [59,60,61] |
miR-25 ↓ | - Diabetic rat streptozotocin-induced | NOX-4 ↑ | Upregulation of NOX-4 promotes oxidative stress | DN | [62] |
miR-146a ↓ | - Human Umbilical Vein Endothelial Cells (HUVECs) | NOX-4 ↑ | Upregulation of NOX-4 promotes oxidative stress | DV | [63,64] |
miR-205 ↓ | - HK-2 cell line | PHD1/EGLN2 ↑ | Upregulation of PHD1/EGLN2 modulates intracellular ROS level and ER stress state | DN | [65] |
miR-192miR-216a miR-217 ↑ | - C57/Bl6 db/db mice - Mouse mesangial cells | PTEN ↓ | Downregulation of PTEN leads the reduction of MnSOD and its antioxidant activity | DN | [66] |
miR-377 ↑ | - Human MC | SOD-1/SOD-2 ↓ | Physiologic expression of SOD-1-2 protects cells from ROS | DN | [67] |
miR-217miR-377 ↑ | - HUVEC cell line - HEK-293 cell line | HO-1 ↓ | Downregulation of HO-1 leads to impaired metabolization of excessive heme generate during hemolysis | DN | [67] |
miR-185 ↑ | - HUVEC cell line | GPx↓ | Physiologic expression of GPx protects cell from oxidative damage | DC | [68] |
miR-144 ↓ | - C57BL/6 mice diabetic STZ induced | Nrf2 ↓ | Upregulation of Nrf2 reduces apoptosis and improving cardiac function | DC | [69] |
miR-214 ↓ | - Male Sprague Dawley rats diabetic STZ induced - Human HK-2 cell line | UCP2 ↑ | UCP2 inhibition attenuates the effects of miR-214 upregulation on oxidative stress | DN | [70] |
miR-21 ↑ | - HUVEC cell line | KRIT1/NRF2/SOD2↓ | Physiologic expression of KRIT1/NRF2/SOD2 limits ROS damage | DC | [71] |
miR-21 ↑ | - Human plasma | IGT/T2D | [72] | ||
miR-22 ↑ | - C57BL/6 mice diabetic STZ induced - C57BL/6 mice HFD - Rat H9c2 cell line | SIRT-1 ↑ | SIRT-1 upregulation protects from oxidative stress | DC | [73] |
miR-92a ↓ | - C57BL/6 db/db mice - HUVEC | HO-1 ↑ | HO-1 upregulation normalizes ROS generation | DV | [74] |
miR-15a ↑ | - Human plasma | DR | [75] | ||
miR-365 ↑ | - Rat Muller cell line - Sprague Dawley rats | TIMP-3 ↓ | Overexpression of Timp-3 improves Muller cell gliosis and retinal oxidative stress | DR | [76] |
miR-126 ↑ | - C57BL/6 ob/ob mice - Endothelial cells | SIRT-1 ↑/H3K56 deacetylation↓ | Upregulation of SIRT-1 and reduction of H3K56 deacetylation protects cells from ROS | T2D | [77] |
miR-34a ↑ | - db/db mice | SIRT-1 ↓ | SIRT-1 upregulation protects from oxidative stress | T2D | [78] |
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Grieco, G.E.; Brusco, N.; Licata, G.; Nigi, L.; Formichi, C.; Dotta, F.; Sebastiani, G. Targeting microRNAs as a Therapeutic Strategy to Reduce Oxidative Stress in Diabetes. Int. J. Mol. Sci. 2019, 20, 6358. https://doi.org/10.3390/ijms20246358
Grieco GE, Brusco N, Licata G, Nigi L, Formichi C, Dotta F, Sebastiani G. Targeting microRNAs as a Therapeutic Strategy to Reduce Oxidative Stress in Diabetes. International Journal of Molecular Sciences. 2019; 20(24):6358. https://doi.org/10.3390/ijms20246358
Chicago/Turabian StyleGrieco, Giuseppina Emanuela, Noemi Brusco, Giada Licata, Laura Nigi, Caterina Formichi, Francesco Dotta, and Guido Sebastiani. 2019. "Targeting microRNAs as a Therapeutic Strategy to Reduce Oxidative Stress in Diabetes" International Journal of Molecular Sciences 20, no. 24: 6358. https://doi.org/10.3390/ijms20246358